responses of plant community composition and biomass production to warming and nitrogen deposition in a temperate meadow ecosystem

Response of plant community composition and productivity to warming and nitrogen deposition in a temperate meadow ecosystem T.. 11, 6647–6672, 2014 Temperate meadow response to climate c

11, 6647–6672, 2014

Temperate meadow response to climate change

This discussion paper is/has been under review for the journal Biogeosciences (BG).

Please refer to the corresponding final paper in BG if available.

Response of plant community

composition and productivity to warming

and nitrogen deposition in a temperate

meadow ecosystem

T Zhang1,3, R Guo2, S Gao1, J X Guo1, and W Sun1

1

Institute of Grassland Science, Northeast Normal University, Key Laboratory of Vegetation

Science, Ministry of Education, Changchun 130024, China

2

Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of

Agricultural Sciences, Key Laboratory of Dryland Agriculture, Ministry of Agriculture, Beijing

100081, China

3

State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and

Geography, Chinese Academy of Sciences Urumqi 830011, China

Received: 1 March 2014 – Accepted: 15 April 2014 – Published: 7 May 2014

Correspondence to: J X Guo (gjixun@nenu.edu.cn) and W Sun (sunwei@nenu.edu.cn)

Published by Copernicus Publications on behalf of the European Geosciences Union.

6647

11, 6647–6672, 2014

Temperate meadow response to climate change

Climate change has profound influences on plant community composition and

ecosys-tem functions However, its effects on plant community composition and net primary

productivity are not well understood A field experiment was conducted to examine the

effects of warming, nitrogen (N) addition, and their interactions on plant community

5

composition and productivity in a temperate meadow ecosystem in northeast China

Experimental warming significantly increased species richness, evenness and

diver-sity, by contrast, N addition highly reduced species richness, evenness and diversity

Warming reduced the importance value of gramineous species but increased in forbs,

N addition had the opposite effect Warming had a significant positive effect on

below-10

ground productivity, but had a negative effect on aboveground biomass The influences

of warming on aboveground productivity were dependent on precipitation

Experimen-tal warming had little effect on aboveground productivity in the years with higher

precip-itation, but significantly suppressed the growth of aboveground in dry years Our results

suggest that warming had indirect effects on plant productivity via altering water

avail-15

ability Nitrogen addition significantly increased above- and belowground productivity,

suggesting that N is one of the most important limiting factors which determine plant

productivity in the studied meadow steppe Significant interactive effects of warming

plus N addition on belowground productivity were also detected Our observations

re-vealed that climate changes (warming and N deposition) plays significant roles in

reg-20

ulating plant community composition and productivity in temperate meadow steppe

1 Introduction

The mechanisms that determine plant diversity and community composition are the key

issues in ecological studies Results from previous studies have indicated that

sustain-ing ecosystems productivity, stability and multi-functionality in grassland communities

25

requires higher biodiversity (Tilman et al., 2006; Hector and Bagchi, 2007; Zavaleta

11, 6647–6672, 2014

Temperate meadow response to climate change

et al., 2010; Cardinale et al., 2012) Plant diversity and community composition are

determined by biotic and abiotic factors, such as, herbivores, soil microbes and soil

available nutrients (De Deyn et al., 2004; Van Der Heijden et al., 2008; Burns et al.,

2009) Importantly, an increasing number of studies reported that climate change can

alter plant community composition and diversity (Klanderud, 2005; Kardol et al., 2010)

5

Global surface temperature has increased at a rate of 0.2◦C per decade over the

past 30 years due to rising greenhouse gas emissions (Hansen et al., 2006), and

global warming is expected to increase continually in the next 100 years (IPCC, 2007),

severely affecting terrestrial ecosystems Several consequences of global warming on

terrestrial plant ecosystem stability includes significant decreased in species richness

10

and diversity (Rull and Vegas-Vilarrúbia, 2006; Fonty et al., 2009; Yang et al., 2011)

Studies found that different functional groups have differential response to warming

(Fay et al., 2011) as well as its profound influence on plant productivity (Hutchings and

de Kroon, 1994; Natali et al., 2012) However, some studies through non-intrusive field

experiments showed that plant responses to warming are those ecosystems

depen-15

dent, with plants in cold-wet northern sites more sensitive to warming (Penuelas et al.,

2004), while warming in other ecosystems decreased productivity of both above- and

belowground biomass (Ciais et al., 2005; De Boeck et al., 2008)

The increase of atmospheric nitrogen (N) deposition induced by human activities

has been recognized as another important threat to terrestrial ecosystem that causes

20

the shifts in plant community structure in terrestrial plant community structure (Duprè

et al., 2010) A large number of studies found that N deposition in soil highly reduced

plant diversity and species richness (Zavaleta et al., 2003; Clark and Tilman, 2008;

Song et al., 2011) Some studies, however, demonstrated that N deposition do not

ac-tually changes species richness of the vegetation (Goldberg and Miller, 1990; Huberty

25

et al., 1998), instead, increases plant diversity (Bowman et al., 2006) Moreover, the

ecological impacts of even relatively small N deposition on plant species interactions

at species level are still not well understood (Payne et al., 2013) Hence, nitrogen

avail-ability play a more important role in limiting plant primary productivity than other soil

6649

11, 6647–6672, 2014

Temperate meadow response to climate change

available nutrients elements, and nitrogen deficiency is globally distributed (LeBauer

and Treseder, 2008; Norby et al., 2010) In general, the response of grassland

pro-ductivity to N deposition is determined whether the soil has reached N saturation or

not Small amounts N deposition can improve plant productivity before soil N reaching

saturation point (Hutchings and de Kroon, 1994; LeBauer and Treseder, 2008), while

5

N deposition can also reduce plant productivity when the soil had reached N saturation

point (Magillet al., 2000)

It is predicted that the temperature will elevate by 2.8–7.5◦C in the next 100 years

in Songnen grassland in northeast China (IPCC, 2007) Although, some previous

stud-ies focused on the effects of warming on plant competitive hierarchy (Niu and Wan,

10

2008) and soil N cycling (Ma et al., 2011) in temperate grassland ecosystem in

north-ern China, the influence of warming on plant community composition and productivity

remains unclear Liu et al (2011, 2013) reported that N deposition significantly

in-creased in China in the last three decades, which had affected agriculture and

grass-land ecosystems Studying the mechanisms that N deposition alter plant community

15

composition, especially the effects of interactions between N deposition and other

global change factors are still not well understood In order to ascertain the potential

effects of climate warming and increased in N deposition on plant community

com-position and productivity, we conducted a field experiment with manipulated warming

and N addition In this experiment, we aim to answer the following questions: (1) how

20

does warming and N addition affects plant community composition and productivity in

temperate meadow ecosystem? (2) The influences of abiotic (e.g soil moisture) and

bi-otic factors (plant interspecific interactions) on plant community and productivity under

climate warming and N addition conditions

11, 6647–6672, 2014

Temperate meadow response to climate change

The experiment was conducted at the Songnen Grassland Ecological Research

Sta-tion (44◦450N, 123◦450E), Northeast Normal University, Jilin Province, northeastern

China The grassland is situated at the eastern edge of the Eurasian steppe and is

5

characterized as Eurasian continental meadow steppe Mean annual precipitation is

approximately 400 mm with 90 % occurs from May to October Annual average air

tem-perature is 4.9◦C, and annual average land surface temperature is 6.2◦C The soil in

the studied area is a soda-saline type, and has pH of 8.2, with 3–4 % organic

mat-ter in the surface layer Vegetation in the experimental site is dominated by Leymus

10

chinensis, Kalimeris integrifolia, Carex duriuscula and Rhizoma phragmitis.

2.2 Experimental design

We used a complete randomized block factorial experimental design with two factors:

warming and N addition There were four treatments: control (C), warming (W), N

addi-tion (N), and warming plus N addiaddi-tion (W+ N), and replicated 6 times The size of each

15

plot was 2 m × 3 m All the warmed plots were heated continuously by infrared radiators

(MSR-2420, Kalglo Electronics Inc Bethlehem, PA, USA) suspended in 2.25 m over

the plot center In each control or N addition plots, one “dummy” heater with the same

shape and size was installed to mimic the shading effects of the infrared radiator All the

heaters under the warming treatments were set at a radiation output of approximately

20

1700 W It is estimated that anthropogenic N deposition is up to 80–90 g m−2yr−1 and

even higher N deposition would occur in the future owing to land-use change and

ac-tivities (He et al., 2007; Liu et al., 2013) In the northern temperate grassland

ecosys-tem the community saturation of N deposition rates was approximately 10.5 g m−2yr−1

(Bai et al., 2010), though atmospheric N deposition was only 2.7 g m−2yr−1 in the last

25

decade in this area (Zhang et al., 2008) Thus, in the N addition treatments plots,

am-6651

11, 6647–6672, 2014

Temperate meadow response to climate change

monium nitrate (10 g m−2yr−1) was added as a pulse of aqueous on the first day in May

every year In the control and warming plots, the same amount of water (without N)

as the N addition treatment was added to account for N addition induced differences in

water availability The experiment started in May 2006 and finished in September 2009

2.3 Meteorological data collection

5

The monthly mean temperature and precipitation from 2006 to 2009 were recorded

using an eddy covariance system installed 200 m apart from the experimental site

One probe of EM50/R (Decagon Ltd, Pullman WA, USA) was buried 0–15 cm from

the soil surface in each experimental plots, measuring soil temperature (ST) and soil

moisture (SM) one hour interval

10

2.4 Plant diversity and productivity

During the growing season, we sampled abundance, height, frequency, and cover of

all plant species found within 1 m × 1 m subplot in each plots The number of plant

species present in the quadrat was recorded as the species richness Plant numbers

per species were also used to calculate importance value (IV), species richness,

species Importance values per species were calculated using the following formula

11, 6647–6672, 2014

Temperate meadow response to climate change

Where RC is relative cover, RF is relative frequency, and RD is relative density

Aboveground biomass was calculated using linear regression model (Bai et al.,

2007) Ten plots beside the experimental plots were randomly selected The cover and

biomass of every species in each plot were observed and constructed a regression

equation Aboveground biomass in each of the experimental plots was then calculated

5

using the regression equation

Belowground biomass was estimated using ingrowth core method Two holes (7 cm

diameter, 50 cm height) were drilled randomly in each plot using soil drill The collected

soil were sieved to remove roots, and placed it into a nylon mesh bags (the size of each

bags were similar to the holes of soil driller) Then the nylon mesh bags were carefully

10

placed into the holes in experiment plots The nylon mesh bags were harvested in 18

July every year The roots in each mesh bags were selected out, washed, and dried at

65◦C for 48 h

2.5 Statistical analysis

All data analyses were performed using SPSS 16.0 (SPSS for Windows, Chicago, IL,

15

USA) A General Linear Model (GLM) following a Duncan test was used to examine the

effects of N addition, warming and experimental year on biomass, importance value,

evenness, and diversity The experimental year was considered as an independent

factor

3 Results

20

3.1 Soil temperature and moisture content

Experimental warming had significant effects on soil temperature (ST) and soil moisture

content (SM) across the 4 experimental years Warming significantly elevated ST (P <

0.05) and reduced SM (P < 0.05) Compared to the control treatment, the mean annual

ST was 1.71◦C and 0.58◦C greater in the warming plots and warming plus N addition

25

6653

11, 6647–6672, 2014

Temperate meadow response to climate change

plots, respectively; whereas it was 0.62◦C lower in the N addition plots (Fig 1a) During

the 4 experimental years, apparent interannual variation was observed in SM (0–15 cm)

(Fig 1b) Compared with the control treatment, experimental warming and warming

plus N addition treatments caused a reduction in the average SM by 11.5 % and 19.8 %,

respectively; whereas the N addition treatment increased the average SM by 5.3 %

5

3.2 Species richness, evenness and diversity

At the early stages of the experiment (in 2006), warming and N addition did not alter

species richness, evenness (Pielou index, E ) and diversity (Shannon–Wiener index,

H) With the progress of warming and N addition treatments, species richness, E and

H were altered significantly (Fig 2).

10

In N addition plots, species richness reduced by an average of 15.8 % (P < 0.05)

an-nually compared to the control plots from 2007 to 2009 (Fig 2a) Warming enhanced

species richness by an average of 11.6 % (P < 0.05) across the four experimental years

(Fig 2a) No interactive effects between warming and N addition on species richness

were detected (P = 0.08) However, there were interactive effects between

experimen-15

tal years and warming on species richness (P < 0.05; Table 2) There was strong

in-terannual variability in E (P < 0.01) with the highest (0.71) in 2009 across all the

treat-ments (Fig 2b) Experimental warming (P = 0.09), as well as warming plus N addition

(P = 0.055) had no effects on E across the four experimental years.

N addition treatment caused a reduction in H by 15.8 % (P < 0.05) and 16.7 % (P <

20

0.05) in 2008 and 2009, respectively (Fig 2c) Warming enhanced H by 16.5 % (P <

0.05) in 2009; however it did not affect H in other experimental years In warming plus

N addition treatment plots, H averagely reduced by 17.6 % (P < 0.05) compared to the

control treatment across the four experimental years

11, 6647–6672, 2014

Temperate meadow response to climate change

During the four experimental years, the importance value (IV) of gramineous (P < 0.01)

and forbs (P < 0.01) showed significant interannual variation (Table 2) N addition

sig-nificantly decreased IV of gramineous by 18.1 % (P < 0.01) in 2006 and enhanced it

5

and 2009 Compared to the control treatment, IV of forbs in N addition plots increased

by 34.1 % (P < 0.05) and 11.1 % in 2006 and 2007, respectively; however it was

re-duced by 11.5 % in 2009 (P < 0.05) Despite warming had no effects on IV of

grami-neous in 2006 and 2007, it caused a reduction in IV by 11.8 % (P < 0.05) and 17.4 %

(P < 0.05) in 2008 and 2009, respectively The IV of forbs in warming plots improved

10

13.6 % (P < 0.05) compared to control treatment in 2007 (Fig 4) In warming plus N

addition treatment, IV of gramineous species improved by 11.5 % (P < 0.05) compared

with control treatment in 2008 There were main effects of experimental years, N

ad-dition, and interactive effects of warming plus N addition on IV of gramineous species

(P < 0.01) (Table 2) Interactive effects of years × N addition, warming × N addition on

15

IV of forbs were observed (P < 0.05) (Table 2) The IV of gramineous species were

higher than forbs across the four treatments from 2006 to 2008; however the IV of

forbs was greater than gramineous in 2009 (Fig 3)

3.4 Aboveground and belowground biomass

Aboveground biomass showed apparent interannual variation, with the highest

20

(394.8 g m−2) and lowest (270.2 g m−2) values in 2006 and 2007, respectively (Fig 4a)

On average, N addition increased aboveground biomass by 20 % (P < 0.01) compared

to the control plots from 2006 to 2009 Warming decreased aboveground biomass by

9.2 % (P < 0.05) and 16.6 % (P < 0.05) in 2006 and 2009, respectively; but it increased

aboveground biomass by 20.8 % (P < 0.05) in 2008 Interactive effects between

warm-25

ing and N addition on aboveground biomass (P < 0.05) were only observed in 2006.

6655

11, 6647–6672, 2014

Temperate meadow response to climate change

Mean belowground biomass across the four treatments in 2006 was much higher

than the other three experimental years (Fig 4b) From 2006 to 2009, N addition

in-creased the belowground biomass by 6.1 % (P < 0.05) on average Warming treatment

5

showed no effects on belowground biomass in 2006; however it increased the

below-ground biomass by 11.2 % (P < 0.05) in 2007, 2008 and 2009 Warming plus N addition

enhanced the belowground biomass by 50.7 % (P < 0.05) across the four experimental

years There were significant effects of year, N addition and interactive effects between

warming and N addition on belowground biomass (Table 2)

10

4 Discussion

4.1 E ffects of experimental warming and N addition on plant community

composition

In the present study, the plant community composition was altered significantly after

four years’ of warming and N addition treatments Warming induced a significant

in-15

crease in species richness in the studied meadow steppe community, which is in

ac-cordance with the results observed in temperate grasslands (Harmens et al., 2004;

Yang et al., 2011) and annual grassland (Zavaleta et al., 2003); however, it was

in-consistent with the results of some other researches where warming was associated

with larger species loss (Klein et al., 2004; Gedan and Bertness, 2009) We found

20

that warming significantly increased species number of forbs, which might be related

to warming induced by changes in soil moisture Warming aggravated

evapotranspira-tion and reduced soil moisture, which are likely caused gramineous species to allocate

more biomass to belowground (Wang et al., 2010), and subsequently suppress the

growth of aboveground biomass, so that the competition ability of gramineous species

25

declined and the increased the competition ability of forbs species

11, 6647–6672, 2014

Temperate meadow response to climate change

In contrast to the significant enhancement effects of warming on species richness

at the community level, N addition reduces species richness This observed reduction

in species richness under the N addition treatment is in agreement with the results

obtained in a prairie grasslands (Clark and Tilman, 2008), a California annual grassland

(Zavaleta et al., 2003), in European acidic grasslands (Stevens et al., 2004; Duprè

5

et al., 2010), and a savannah grassland (Isbell et al., 2013) In the studied temperate

steppe (dominated by a perennial grass L chinensis), productivity is often limited by N

availability (Bai et al., 2010) In general, gramineous species are sensitive to N (Foster

and Gross, 1998); therefore N addition significantly improved the growth and cover of

gramineous species and suppresses the growth of other species (e.g Leguminosae,

10

Compositae, etc.)

Current empirical and theoretical ecological results suggest that many species could

be at risk and plant diversity would decline with the continuation of global warming

(Botkin et al., 2007) The experimental warming associated with loss of plant diversity

were detected in many ecosystems, such as in moist tussock tundra (Chapin III et al.,

15

1995), and in New England salt marshes (Gedan and Bertness, 2009) However, there

are some other studies reported that plant diversity was not significantly affected by

warming (Harmens et al., 2004; Yang et al., 2011) In our study, although warming did

not affect plant diversity from 2006 to 2008, the diversity increased dramatically in the

warming plots in the fourth experimental year (Fig 4) These results may be partly

as-20

cribed to the reduction of competitive dominant species L chinensis and improved the

survival of other species (such as, Compositae, Leguminosae) This can be explained

based from similar previous results that climate change indirectly affects co-existing

species via affecting dominant species (Engel et al., 2009; Kardol et al., 2010) While

no significant effects of N addition on plant diversity was observed during the first two

25

experimental years, and subsequently found significant effects in 2008 and 2009, which

are in agreement with the results of previous observations in many terrestrial

ecosys-tems (Pennings et al., 2005; Bobbink et al., 2010) N addition improved the growth

condition of L chinensis, which subsequently reduced the survival space of other

co-6657

11, 6647–6672, 2014

Temperate meadow response to climate change

existing species Furthermore, no decline of species richness, evenness and diversity

under N addition at the early two experimental years, which might be related to the

soil N availability, in Songnen meadow steppe with total N (2 g kg−1) and available N

(40 mg kg−1) is much lower, which limited the survival of annual forbs A small quantity

or short-term of N deposition can not affect plant diversity, but long-term N deposition

5

might significantly reduce plant diversity and ecosystems stability In the present study,

significant decline of plant diversity in warming plus N addition treatment in 2008 and

2009 was observed The result might suggest that the changes of plant diversity are

de-termined by the effects of many global changes The influence of long-term integrated

environmental factors on plant diversity should be further investigated

10

Changes in importance values (IV) of species can reflect the variation of plant

com-munity composition We found that the IV of gramineous species were much higher

than forbs from 2006 to 2008, but the IV of forbs species were greater than

grami-neous species in 2009 N addition highly improved the IV of gramigrami-neous species, while

warming decreased it and increased importance value of forbs (Table 2) The

signif-15

icant influence of experimental years, N addition, interaction between years and N

addition on importance of gramineous and forbs species (P < 0.05) might be due to

the improved growth of L chinensis and Phragmites australis, and reduced the

pro-portion of forbs, whereas warming restrained the growth of gramineous species These

observations in this study highlights that climate changes have the potential to alter

20

species interactions However, many studies have demonstrated that climate change

can also influence the composition of insects and soil microorganisms (Liu et al., 2009;

Potts et al., 2010), which subsequently can also alter plant species interactions

(Bidart-Bouzat and Imeh-Nathaniel, 2008; Singh et al., 2010) Up to now, climate changes

associated with interactions between soil microorganisms and plant species, and the

25

influence of interactions of belowground and aboveground on plant community

compo-sition are remained to be studied

11, 6647–6672, 2014

Temperate meadow response to climate change

Nitrogen is one of the most essential elements for the development of plant species,

N limit often determines terrestrial ecosystem net primary productivity (Elser et al.,

2007; LeBauer and Treseder, 2008) Several published papers documented that N

in-5

put increased aboveground productivity, such as in a high plateau near Julier Pass in

the central Alps (Bassin et al., 2007), a temperate old field in Canada (Hutchison and

Henry, 2010) Our results showed that N addition significantly increased the

above-ground net primary productivity, which is consistent with the results of previous studies

Plant species can quickly respond to nutrient availability, especially for N (Hutchings

10

and de Kroon, 1994) When soil available N increased, growth of plants will greatly

im-prove and imim-prove the total aboveground biomass in this area Furthermore, the effect

of N deposition on plant productivity is influenced by soil moisture Model simulation

results suggest that N addition improved ecosystem productivity when soil moisture

were high, whereas it has no effects on ecosystem productivity when soil moisture was

15

lower in semiarid ecosystem (Asner et al., 2001) In fact, we observed that the effects

of N addition on aboveground biomass in the years of abundant rain were much higher

than other years

Significant decline in aboveground biomass induced by experimental warming was

detected in semiarid ecosystem in Songnen meadow steppe except in 2008 Our

ob-20

servations is in accordance with the results of some studies from annual grasslands

(Zavaleta et al., 2003), an old field site (Hutchison and Henry, 2010), in Europe wide

(Ciais et al., 2005) These results may be partly ascribed to thermal damage by

warm-ing in summer (June to August) (Wang et al., 2010) In general, the hydrothermal

con-dition in summer is good for plant growth, but high temperature beyond plant capacity

25

will severely affect the growth of plant species (Wan et al., 2005) No significant effects

of warming on the belowground biomass were observed, which was consistent with

the previous results (Sebastiá et al., 2004) Despite warming plus N addition treatment

6659